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La-Llave-León et al. BMC Public Health (2016) 16:1231 DOI 10.1186/s12889-016-3902-3

RESEARCH ARTICLE

Open Access

The relationship between blood lead levels and occupational exposure in a pregnant population Osmel La-Llave-León1*, José Manuel Salas Pacheco1, Sergio Estrada Martínez1, Eloísa Esquivel Rodríguez2, Francisco X. Castellanos Juárez1, Ada Sandoval Carrillo1, Angélica María Lechuga Quiñones1, Fernando Vázquez Alanís3, Gonzalo García Vargas4, Edna Madai Méndez Hernández1 and Jaime Duarte Sustaita4

Abstract Background: Pregnant women exposed to lead are at risk of suffering reproductive damages, such as miscarriage, preeclampsia, premature delivery and low birth weight. Despite that the workplace offers the greatest potential for lead exposure, there is relatively little information about occupational exposure to lead during pregnancy. This study aims to assess the association between blood lead levels and occupational exposure in pregnant women from Durango, Mexico. Methods: A cross-sectional study was carried out in a population of 299 pregnant women. Blood lead was measured in 31 women who worked in jobs where lead is used (exposed group) and 268 who did not work in those places (control group). Chi-square test was applied to compare exposed and control groups with regard to blood lead levels. Odds ratio (OR) and 95% confidence intervals (CI) were calculated. Multivariable regression analysis was applied to determine significant predictors of blood lead concentrations in the exposed group. Results: Exposed women had higher blood lead levels than those in the control group (4.00 ± 4.08 μg/dL vs 2.65 ± 1.75 μg/dL, p = 0.002). Furthermore, women in the exposed group had 3.82 times higher probability of having blood lead levels ≥ 5 μg/dL than those in the control group. Wearing of special workwear, changing clothes after work, living near a painting store, printing office, junkyard or rubbish dump, and washing the workwear together with other clothes resulted as significant predictors of elevated blood lead levels in the exposed group. Conclusions: Pregnant working women may be at risk of lead poisoning because of occupational and environmental exposure. The risk increases if they do not improve the use of protective equipment and their personal hygiene. Keywords: Blood lead, Occupational exposure, Pregnant women, Risk factors

Background Lead has been clearly shown to be a neurotoxic agent widely distributed in the environment [1]. Excessive lead exposure may occur in the workplace. Some jobs that expose people to lead include: mining, smelting, foundry work, construction, plumbing, radiator manufacturing, * Correspondence: [email protected]; [email protected] 1 Instituto de Investigación Científica, Universidad Juárez del Estado de Durango, Avenida Universidad esq. con Volantín, Zona Centro, C.P. 34000 Durango, DGO, Mexico Full list of author information is available at the end of the article

lead-acid battery recycling, manufacturing of rubber products, and the chemical industry. Years ago, lead was also used regularly in paint, ceramics, and pipe solder among other things. Because of its potential health problems, the amount of lead used in these products today has lessened or has been removed. However, lead is still common in many industries, including construction, mining, and manufacturing [2]. Lead can harm many of the body’s organ systems. Human exposure to lead can result in a wide range of biological effects [3]. It is well known that childhood and

© The Author(s). 2016 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

La-Llave-León et al. BMC Public Health (2016) 16:1231

pregnancy are the most sensitive population to lead exposure. A pregnant woman with an elevated blood lead concentration may expose her fetus to the toxic effect of lead. Elevated blood lead levels (BLLs) in children cause learning and behavioral deficits [4, 5]. Low-level lead exposure, including prenatal exposure, has been linked to decreased performance on IQ tests for school children [6–9]. Several studies have suggested that any level of exposure is potentially detrimental and no threshold for these effects has been identified [10, 11]. Lead concentrations have declined in the last decades due to the increase in health interventions [12]. In spite of this, lead exposure remains a risk factor for female reproductive health, even at low levels of lead in blood [13]. Once absorbed from the gastrointestinal tract or the respiratory system, lead is transported bound to erythrocytes and accumulates in bone [14]. During pregnancy, calcium demands increase. This leads to increased bone turnover, with a consequential release of lead from bone and increased blood lead levels [15, 16]. Lead can cross the placenta and expose the fetus to the harmful effects of this toxic, thus affecting the embryonic development of multiple organs and causing neurobehavioral impairments in infancy and early childhood [4, 5, 9, 17]. Therefore, pregnancy is considered a critical time for exposure to lead for the mother and the fetus [14, 18]. Over the past several decades there has been a remarkable reduction in environmental sources of lead and a decreasing trend in the prevalence of elevated blood lead levels [2]. However, some reproductive health damages at levels of lead in blood below 10 μg/dL have been reported. Therefore, in recent years, many studies have focused on the health effects at low levels of lead in blood. Low blood lead concentrations in pregnant women have been associated with miscarriage [19, 20], pregnancy hypertension, or preeclampsia [12, 21–24] premature delivery [13], premature rupture of the membranes [25], and low birth weight [26, 27]. On the other hand, it is considered that leadrelated toxicity can occur at levels as low as 5 μg/dL [28]. Hence, maternal exposure to lead plays an important role in adverse pregnancy outcomes. Despite that the workplace offers the greatest potential for lead exposure, there is relatively little information about the occupational exposure to lead during pregnancy. It is necessary to identify sources of lead exposure relevant to this population. Some of the jobs that commonly involve lead exposure are battery manufacture or repair; construction (welding or cutting lead-painted metal); radiator manufacture or repair; wire cable cutting and manufacture, and cable, battery, or scrap metal salvage, plating operations; manufacturing or using leaded paints, dyes or pigments, or lead soldering in the electronics industry, among others [29]. In Mexico, and in other developing countries, it is common to find pregnant

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women working in places with potential sources of lead exposure. The aim of this study was to assess the association between blood lead levels and occupational exposure in pregnant women from Durango, Mexico.

Methods Study population

From June 2007 to May 2008 a cross-sectional study was conducted to evaluate the association between BLLs and some risk factors in pregnant women who received health attention in the State of Durango, Mexico [30]. The study population consisted of pregnant women who received medical attention in two sanitary jurisdictions pertaining to the Secretary of Health. The total estimated number of pregnant women seen in these two jurisdictions during a 1 year period was obtained from the Secretariat of Health databases, and the sample required was distributed equally in 12 municipalities. The participants were recruited from Obstetrics and Gynecology Departments of the municipal hospitals. All women who presented for prenatal care on the days that the study team visited, independent of their gestational age, were asked to participate in the study if they met the inclusion criteria. The inclusion criteria were: being pregnant, living in Durango, able to understand Spanish, and receiving health care paid for by the Secretary of Health. Each municipality was visited two or three times during the recruitment period, until the sample size was completed. Of the 337 pregnant women who presented for prenatal care on the days of the visits, 12 women were excluded because they did not live in Durango and 26 declined to participate in the study. A total of 299 women were included in the study (Aditional file 1). The interviewer’s interaction with patients was standardized. All patients gave their informed written consent and answered a set of questions in a face-to-face interview. The research protocol was approved by the Ethical Committee of Durango General Hospital. First, the group was treated as a cohort. After that, a regression with lead levels as outcome allowed to attribute the proportion of risk from occupational and nonoccupational exposure. For assessment of the association between blood lead levels and occupational exposure, subjects were classified into two groups: women who worked in places where lead is used (exposed group) and women who did not work in those places (control group). Women who worked in automotive repair shops, mining laboratories, welding workshops, automotive harness factories, hairdressing salons, and road sweepers were included in the exposed group. Unemployed women and those women who had a job where leadcontaining materials are not used, were included in the control group.

La-Llave-León et al. BMC Public Health (2016) 16:1231

Blood lead measurement

Blood samples were collected using lead-free tubes containing EDTA. Samples were stored in the original tube at 4o C before being transferred to the Environmental Toxicology Laboratory, Faculty of Medicine, Juarez University of Durango State. The time between receipt and analysis varied from 1 to 3 weeks. During which time, the specimens were stored refrigerated at 4 °C. Lead concentration was determined by graphite furnace atomic absorption spectrometry. Bovine blood obtained from the National Institute of Standards and Technology (NIST) was used as standard reference material. Statistical analysis

Data were analyzed to describe demographic characteristics, BLLs, and potential sources of lead exposure. The normality of the variables was tested using the Kolmogorov-Smirnov test. BLLs were log-transformed prior to analysis. Multivariable regression analysis was conducted to determine the proportion of risk from each occupational and non-occupational exposure. After that, the study population was divided into two groups according to occupation (occupationally exposed and nonoccupationally exposed). Student t-test was applied for comparison of quantitative variables. Chi-square test was applied to compare exposed and control groups regarding blood lead levels (BLLs ≥ 5 μg/dL vs BLLs < 5 μg/dL). Odds ratio (OR) and 95% confidence intervals were calculated. To identify non-occupational sources of lead exposure for pregnant women we explored the following: the way in which workwear is washed (together with other clothes or alone), use of lead-glazed pottery, use of hair dyes, living near workplaces where lead is used (mining zones, battery workshops, junkyards, rubbish dumps and painting workshops), pica behavior and living with someone who works with lead, in both exposed and control groups. These activities have been documented to be lead-related. Chi-square test was also used to compare both groups regarding nonoccupational sources of lead exposure. Student t-test was also used to compare blood lead levels according to some protection habits in the exposed group. Use of respiratory protective equipment, habit of wearing gloves, wearing of special workwear, handwashing before eating, changing clothes after work, and use of any protective equipment were analyzed as dichotomous variables. Finally, backward stepwise multivariable regression analysis was applied to determine significant predictors of blood lead concentrations in the exposed group. A set of variables selected on the basis of previous knowledge or because of associations with lead levels in bivariate analyses (at p < 0.25) were entered into the model. The full model was followed by stepwise backward elimination to

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determine whether each variable remained significant after non-significant covariates were excluded. All statistical analyses were performed using SPSS for Windows statistical package version 15.0. A p-value < 0.05 was considered statistically significant.

Results The mean blood lead concentration in the study population was 2.79 μg/dL (SD 2.14), geometric mean 2.38 μg/ dL, 95% CI (2.25 – 2.54). Among the 299 pregnant women enrolled in the study, 31 (10.4%) worked in places where lead is used, and 268 (89.6%) did not work where lead-containing materials are used (Table 1). Results of multiple linear regression on association between blood lead levels and risk factors are shown in Table 2. Living in a mine zone was associated with increased blood lead (p = 0.044). However, working in places where lead is used was the main factor associated with blood lead concentration. On the basis of this result, the study population was divided into two groups: exposed and non-exposed. Table 3 summarizes the main characteristics of both groups. There were no significant differences between the groups regarding age, gestational age, number of pregnancies, body mass index (BMI), hemoglobin and monthly income per person. However, the blood lead concentration of the exposed group was significantly higher than that of the control group (p = 0.002). Frequency of BLLs ≥ 5 μg/dL is depicted in Table 4. The proportion of women with BLLs ≥ 5 μg/dL in the exposed group was significantly higher compared to the control group (22.6% vs 7.1%; p < 0.01). In addition, women in the exposed group had 3.8 times more Table 1 General information and blood lead levels of study population (N = 299) Variables

Percent

Mean (SD)

Age (years)

24.32 (6.71)

Gestational age (weeks)

24.07 (8.68)

Pregnancies

2.0 (1.0)

Body mass index (kg/m2)

27.23 (5.63)

Hemoglobin (g/dL)

12.55 (1.34)

Monthly income per person, USD

140.95 (144.73)

Working in places where lead is used Yes

10.4

No

89.6

Blood lead levels (μg/dL)

2.79 (2.14)

Geometric mean (95% CI)

2.38 (2.25 – 2.54)

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Table 2 Results from the multiple linear regression analysis on the association between blood lead and risk factors Risk factor

Coefficient β

Washing the workwear together with other clothes

95% CI

p

0.106

- 0.018 – 0.229

0.093

0.033

- 0.102 – 0.168

0.634

Dyeing hair

- 0.016

- 0.147 – 0.115

0.813

Living near workplaces where lead is used

- 0.021

- 0.197 – 0.156

0.818

0.237

0.006 – 0.468

0.044

Living near battery workshop

- 0.016

- 0.209 – 0.177

0.869

Living near junkyard

- 0.079

- 0.284 – 0.127

0.452

Living near rubbish dump

0.141

- 0.060 – 0.342

0.169

Living near straightening and painting workshop

0.023

- 0.172 – 0.218

0.819

Pica behavior

0.115

- 0.032 – 0.261

0.124

Living with someone who works with lead

0.056

- 0.071 – 0.183

0.387

Living near painting store

0.081

- 0.167 – 0.329

0.521

Living near printing office

- 0.120

- 0.441 – 0.201

0.461

0.306

0.103 – 0.509

0.003

Use of lead glazed pottery

Living near mining zone

Working in places where lead is used R2 = 0.082

probability to have BLLs above 5 μg/dL than those in the control group. Non-occupational sources of lead exposure for exposed and control groups are summarized in Table 5. The proportion of women who had the habit of dyeing their hair was significantly higher in exposed women when compared to the control group (p = 0.010) and the same was observed in the exposed group regarding living near workplaces where lead is used when compared with control women (p = 0.043). However, there were no significant differences in other variables between the compared groups. To evaluate the influence of some work conditions on blood lead levels in the exposed group, some protection habits were explored (Table 6). Blood lead levels were significantly higher in women who did not wear special

workwear (p = 0.028) and in those who did not have the habit of changing clothes after work (p = 0.025). Table 7 displays potential sources of blood lead in the exposed group. After multivariable analysis, seven variables were retained in the final model: wearing of special workwear, changing clothes after work, living near a painting store, living near a printing office, living near a junkyard, living near a rubbish dump and washing the workwear together with other clothes. These variables accounted for 86.5% of the total variance. The model was adjusted by age, educational level and gestational age.

Discussion In this cross-sectional study, we examined the association of blood lead levels with occupational exposure in pregnant women. The blood lead levels in our

Table 3 General information and blood lead levels of the exposed subjects and control groupa Variable

Exposed group (n = 31)

Control group (n = 268)

p value*

Age (years)

26.03 (6.17)

24.13 (6.76)

0.135

Gestational age (weeks)

22.71 (8.06)

24.22 (8.75)

0.358

Number of pregnancies

2.55 (1.38)

2.23 (1.47)

0.253

Body mass index (kg/m2)

28.81 (4.79)

27.04 (5.70)

0.098

Hemoglobin (g/dL)

12.97 (1.11)

12.50 (1.36)

0.065

Monthly income per person, USD

165.62 (130.59)

138.00 (146.28)

0.316

Blood lead levels (μg/dL)

4.00 (4.08)

2.65 (1.75)

0.002**

a

Values shown as mean (standard deviation) p value was calculated from Student t-test ** p value from Log BLL *

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Table 4 Frequencies of BLL ≥ 5 μg/dL in the study population Subjects

BLLs ≥ 5 μg/dL n (%)

BLLs